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High Contents of Very Long-Chain Polyunsaturated Fatty Acids in Different Moss Species

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High Contents of Very Long-Chain Polyunsaturated Fatty Acids in Different Moss Species Plant Cell Rep (2014) 33:245–254 DOI 10.1007/s00299-013-1525-z ORIGINAL PAPER High contents of very long-chain polyunsaturated fatty acids in different moss species Anna K. Beike • Carsten Jaeger • Felix Zink • Eva L. Decker • Ralf Reski Received: 23 August 2013 / Revised: 19 September 2013 / Accepted: 8 October 2013 / Published online: 30 October 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com Abstract organism Physcomitrella patens, tissue-specific differences Key message Mosses have high contents of polyunsat- in the fatty acid compositions between the filamentous urated fatty acids. Tissue-specific differences in fatty protonema and the leafy gametophores were observed. acid contents and fatty acid desaturase (FADS)-encod- These metabolic differences correspond with differential ing gene expression exist. The arachidonic acid-syn- gene expression of fatty acid desaturase (FADS)-encoding thesizing FADS operate in the ER. genes in both developmental stages, as determined via Abstract Polyunsaturated fatty acids (PUFAs) are microarray analyses. Depending on the developmental important cellular compounds with manifold biological stage and the species, AA amounts for 6–31 %, respec- functions. Many PUFAs are essential for the human diet tively, of the total fatty acids. Subcellular localization of and beneficial for human health. In this study, we report on the corresponding FADS revealed the endoplasmic reticu- the high amounts of very long-chain (vl) PUFAs (CC20) lum as the cellular compartment for AA synthesis. Our such as arachidonic acid (AA) in seven moss species. results show that vlPUFAs are highly abundant metabolites These species were established in axenic in vitro culture, as in mosses. Standardized cultivation techniques using pho- a prerequisite for comparative metabolic studies under tobioreactors along with the availability of the P. patens highly standardized laboratory conditions. In the model genome sequence and the high rate of homologous recombination are the basis for targeted metabolic engi- neering in moss. The potential of producing vlPUFAs of Communicated by P. Kumar. interest from mosses will be highlighted as a promising Electronic supplementary material The online version of this area in plant biotechnology. article (doi:10.1007/s00299-013-1525-z) contains supplementary material, which is available to authorized users. Keywords Physcomitrella patens Á Polyunsaturated A. K. Beike Á F. Zink Á E. L. Decker Á R. Reski (&) fatty acids Á Arachidonic acid Á In vitro cultivation Á Plant Biotechnology, Faculty of Biology, University of Freiburg, Mosses Á Metabolite profiling Scha¨nzlestraße 1, 79104 Freiburg, Germany e-mail: [email protected] C. Jaeger Introduction Core Facility Metabolomics, ZBSA, Center for Biological Systems Analysis, University of Freiburg, Habsburgerstraße 49, Polyunsaturated fatty acids (PUFAs) are ubiquitous 79104 Freiburg, Germany metabolites with a large variety of biological functions. R. Reski Their functions range from key roles in cellular signaling BIOSS-Centre for Biological Signalling Studies, as precursors of hormones and phytohormones to the 79104 Freiburg, Germany maintenance of membrane integrity and dynamics as major components of the biomembrane system. Many very long- R. Reski FRIAS-Freiburg Institute for Advanced Studies, 79104 Freiburg, chain (vl) PUFAs (CC20), especially x-3 PUFAs, are Germany beneficial for human health as they contribute to the 123 246 Plant Cell Rep (2014) 33:245–254 prevention of cardiovascular and inflammatory diseases ability to integrate homologous nucleotide sequences into (Calder 2004; Xue et al. 2013). Vl x-6 PUFAs such as the genome, metabolic engineering, but also the production dihomo-c-linolenic acid (DGLA, 20:3D8,11,14) and arachi- of recombinant proteins, has already been realized in P. donic acid (AA, 20:4D5,8,11,14) as well as the x-3 vlPUFA patens (Bu¨ttner-Mainik et al. 2011; Chodok et al. 2012; eicosapentaenoic acid (EPA, 20:5D5,8,11,14,17) are the pre- Parsons et al. 2012). The high rate of homologous cursors of biologically active signaling compounds in recombination in P. patens is unique among land plants at humans, namely, eicosanoid hormones, which comprise the current state of knowledge, being comparable with the prostaglandins, leukotrienes and thromboxanes (Samuels- gene targeting efficiency in yeast and several times higher son 1983; Harizi et al. 2008). Eicosanoid hormones than in vascular plants (Strepp et al. 1998; Schaefer 2001; mediate important physiological processes such as hyper- Hohe et al. 2004; Kamisugi et al. 2006). Beside P. patens, sensitivity reactions and inflammatory responses, but also homologous recombination-based gene targeting is also immunity (Samuelsson 1983; Samuelsson et al. 1987; applicable in the moss Ceratodon purpureus (Bru¨cker et al. Harizi et al. 2008). Furthermore, the semi-essential fatty 2005) and the liverwort Marchantia polymorpha (Ishizaki acid AA plays an important role in infant nutrition, as AA et al. 2013), indicating that this might be a common feature levels correlate with first year growth of preterm infants among certain Bryopsida and liverworts, thus expanding (Carlson et al. 1993). the selection of species to be analyzed with regard to Essential PUFAs for the human diet are linoleic acid genetic engineering and the production of metabolites of (LA, 18:2D9,12), a-(ALA, 18:3D9,12,15) and c-linolenic acid interest. (GLA, 18:3 D6,9,12) that need to be ingested via plant-based To quantify the abundance of vlPUFAs among Bry- nutrition, while nutritional sources for AA and EPA are opsida, comparative fatty acid profiles of seven moss spe- mainly marine fishes (Gill and Valivety 1997). However, cies from different phylogenetic groups were established. alternative sources for AA can also be bacteria, fungi The cellular compartment of AA synthesis is the endo- (Yuan et al. 2002), algae (Bigogno et al. 2002) and mosses plasmic reticulum (ER) as confirmed via green fluorescent (Hartmann et al. 1986; Girke et al. 1998; Kaewsuwan et al. protein (GFP)-tagging of the AA-producing FADS from P. 2006). In contrast to mosses which contain large amounts patens. It has previously been shown that the different of vlPUFAs (Grimsley et al. 1981; Hartmann et al. 1986; developmental stages of P. patens protonema and ga- Girke et al. 1998; Zank et al. 2002; Mikami and Hartmann metophores show distinct metabolic profiles for sugar 2004; Kaewsuwan et al. 2006), higher plants rarely possess derivates, amino acids and nitrogen-rich storage com- these as they lack the corresponding enzymes for vlPUFA- pounds (Erxleben et al. 2012). Here, we established com- synthesis (Gill and Valivety 1997). In the moss model parative fatty acid profiles of protonema and gametophores organism, Physcomitrella patens, the genes that encode the to characterize tissue-specific fatty acid contents. The key enzymes of AA synthesis, namely D6- and a D5-fatty observed differences in the PUFA profiles of protonema acid desaturases (FADS) and a D5-fatty acid elongase have and gametophores were compared with and supported by already been identified via targeted gene replacement and microarray-derived gene expression profiles of putative biochemical characterization (Girke et al. 1998; Zank et al. FADS-encoding genes, which for some FADS-coding 2002; Kaewsuwan et al. 2006). Recently, also two P. genes revealed significantly higher expression levels in patens D12-FADS, that are associated with linoleic acid protonema than in gametophores. biosynthesis, were identified and characterized by heter- ologous expression in the yeast Saccharomyces cerevisiae (Chodok et al. 2013). Materials and methods The high abundance of vlPUFAs, which are uncommon in higher plants, marks clear metabolic differences between Plant material and growth conditions mosses and higher plants. On the one hand the use of moss genes in a transgenic approach, e.g., for the optimization of With the exception of the established laboratory strain of P. oil seed crops as an alternative to the use of genes from patens, the moss species were collected in the field and microalgae or fish (Jiao and Zhang 2013), forms a prom- established in axenic in vitro culture as described in Beike ising research field. On the other hand, mosses themselves et al. (2010). The mosses were axenically cultivated on provide the potential for the discovery of yet uncharacter- modified Knop medium (Reski and Abel 1985) under ized metabolites (Cove et al. 2006; Asakawa 2007; Xie and standardized growth conditions of 55–70 lmol m-2 s-1 Lou 2009; Erxleben et al. 2012), but also for the production light intensity and a photoperiod of 16 h light to 8 h dark at of metabolites in the moss bioreactor that was established 23 ± 1 °C (Hohe et al. 2002). Gametophores were grown for cultivation of P. patens (Decker and Reski 2008, 2012). in Petri dishes that were enclosed with NescofilmTM (Roth, Due to the high rate of homologous recombination, i.e., the Karlsruhe, Germany). For vegetative propagation, the 123 Plant Cell Rep (2014) 33:245–254 247 Fig. 1 Moss species selection. Overview of the moss species grown in axenic in vitro culture and analyzed regarding their fatty acid contents. a Physcomitrella patens, b Encalypta streptocarpa, c Pottia lanceolata, d Plagiomnium undulatum, e Atrichum undulatum, f Brachythecium rutabulum, g Rhynchostegium murale. Scale bar 1mm gametophores were disrupted with forceps and transferred supernatant was transferred to a new tube with a Pasteur to fresh solid medium. The species collection comprises P. pipette. The remaining pellet was re-extracted with fresh patens, Encalypta streptocarpa, Pottia lanceolata, Pla- chloroform–methanol (2:1 v/v; Folch et al. 1957) con- giomnium undulatum, Brachythecium rutabulum, Rhynch- taining 0.01 % BHT for 10 min at room temperature. After ostegium murale and Atrichum undulatum (Fig. 1). For centrifugation, the supernatants were combined, evaporated fatty acid and RNA extraction the plant material was har- under a stream of nitrogen and dissolved in 1.5 mL chlo- vested with forceps and transferred to liquid nitrogen until roform–methanol (2:1 v/v).
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